Climate change models predict southerly shift of the cat flea (Ctenocephalides felis) distribution in Australia

RESEARCH

Climate change models predict southerly

shift of the cat flea (

Ctenocephalides felis

)

distribution in Australia

Nicole Crkvencic and Jan Šlapeta

Abstract

Background: Bioclimatic variables play an integral part in the life-cycle of Ctenocephalides felis, the most common flea found on companion animals. It is essential that we understand the effects of climate on C. felis distribution as fleas are a major veterinary and public health concern. This study investigated the current distribution of C. felis in Australia and future projections based on climate modelling.

Results: Typing of C. felis was undertaken using the cytochrome c oxidase subunit 1 (cox1) mitochondrial DNA (mtDNA) region and current distribution of haplotypes was mapped by Maximum Entropy (Maxent) niche modelling. All C. felis haplotypes have been predicted to persist in environments along the eastern and southern coastlines of Australia and distinct ecological niches were observed for two C. felis haplogroups. Clade ‘Cairns’ haplogroup thrives under the northern coastal tropical conditions whilst Clade ‘Sydney’ haplogroup persists in temperate climates along the eastern and southern coasts. The model was then used to predict areas that are projected to have suitable climatic conditions for these haplogroups in 2050 and 2070 under the Intergovernmental Panel on Climate Change (IPCC) climate change scenarios. Under all IPCC Representative Concentration Pathways (RCP) climate change sce-narios, the geographical range of all haplotypes was reduced by 5.59–42.21% in 2050 and 27.08–58.82% by 2070. The ranges of all clades were predicted to shift south along the eastern coastline.

Conclusions: As future temperatures exceed critical threshold temperatures for C. felis development in the northern tropical areas, Clade ‘Cairns’ haplogroup is predicted to shift south along the coastline and possibly outcompete the temperate haplogroup in these areas. If C. felis haplogroups possess distinct climatic niches it suggests a potential for these to be biologically distinct and have differing developmental rates and vector capabilities.

Keywords: Bioclimatic variables, cox1, Haplotypes, Maxent

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Background

Ctenocephalides felis (Siphonaptera: Pulicidae), com-monly known as the cat flea, is the most common flea found on companion animals in Australia [1, 2]. Cteno-cephalides felis has a cosmopolitan distribution and is highly tolerant to a wide range of environmental condi-tions [3]. As C. felis imposes health risks to humans and domestic animals as a biological vector, it is important to understand and predict both current and future suitable

habitats [3]. Climatic variables play an integral part in the life-cycle of C. felis and consequently have an effect on their distribution, as they will only reside and successfully reproduce within limited climatic ranges [4]. As a result, it is essential that we understand the effects of climate on

C. felis distribution, both now and in the future.

Recent studies have investigated the molecular diver-sity of C. felis in Australia at the cytochrome c oxidase subunit 1 (cox1) and cytochrome c oxidase subunit 2 (cox2) mitochondrial DNA (mtDNA) regions [1, 2, 5–7]. Two genetically distinct subpopulations were identified, with one population located along the eastern and south-ern coasts and the other strictly located in the northsouth-ern

Open Access

*Correspondence: [email protected]

city of Cairns, Australia. It is currently unknown what biological factors are governing these distributions and whether the Cairns subpopulation is restricted to this area.

Climate change is anticipated to alter the ranges of zoonotic parasite species and consequently, associated disease emergence within human and domestic animal populations in the future [4, 8]. The effect of climate change can have the potential to shift tropical popula-tions into temperate areas as bioclimatic norms exceed critical threshold temperatures for parasite survival [9]. In a predictive model study, the distribution of C. felis in Spain was predicted to expand to newly suitable habitats as a result of climate change [10]. This could be the cir-cumstance in Australia, where the distribution of C. felis

subpopulations may shift to newly suitable habitats. Eco-logical niche modelling such as the Maximum Entropy (Maxent) model [8, 11] in epidemiology is a useful tool as it can assess the relative importance of bioclimatic vari-ables and use these factors to predict changes in the dis-tribution of parasites and their pathogens over time [12].

The aim of this study is to model if C. felis distribution in Australia will be affected by the Intergovernmental Panel on Climate Change (IPCC) climate change scenar-ios. To address this aim, we evaluated the genetic diver-sity of the cat flea by polymerase chain reaction (PCR) amplification and sequencing of the cox1 mtDNA region. The predictive Maxent modelling was then used to deter-mine the current and future distribution of C. felis haplo-types in Australia using IPCC climate change scenarios.

Methods Flea specimens

Fleas were collected opportunistically from domes-tic cats and dogs presented to various veterinary clinics across the north-eastern region of Queensland (Addi-tional file 1: Table S1). Fleas from individual animals were collected by veterinarians in 1.5  ml Eppendorf tubes, labelled with the postcode of the veterinary clinic, and stored in 80–100% ethanol at -20  °C for transport to The University of Sydney Veterinary Parasitology Diag-nostic Laboratory. In addition, 65 C. felis samples from previous studies that have been published on GenBank and 33 unpublished C. felis genotyped samples were included (Additional file 1: Table S2) [1, 2, 5]. These addi-tional samples were collected from veterinary clinics in all seven states and territories across Australia and were used to increase the sensitivity of the ecological niche model. There is a limitation in the extent of flea local-ity in this study as samples were collected from dogs or cats presented at veterinary clinics within their local area where these animals have acquired these fleas from an unknown locality.

Morphological identification of flea specimens

Fleas were identified morphologically using a stereo microscope (5–20× objective) with the aid of

identifi-cation keys and descriptions [13, 14].

Extraction of total DNA and mounting of flea exoskeletons Total flea DNA was extracted using an ISOLATE II Genomic DNA kit (Bioline, Eveleigh, Australia) accord-ing to manufacturer’s protocol with a few modifications as previously described [2]. Briefly, an incision was made on the anterior dorsal section of the flea abdomen using a sterile scalpel blade and digested overnight with 25 µl Proteinase K and 180 µl of lysis buffer at 56  °C. The remaining steps were as per manufacturers pro-tocols. The total DNA was eluted into 50 µl of elution buffer and stored at -20 °C until analysis by PCR. Exo-skeletons were placed in 10% potassium hydroxide for 12 h, rinsed with RO water and dehydrated in an etha-nol series (70%, 80%, 95% and 100%) for 1 h each. The specimens were then slide-mounted in Euparal (Aus-tralian Entomological Supplies, Coorabell Australia).

Amplification of the cox1 gene by PCR and sequence analysis

Modelling of current C. felis distribution in Australia using Maxent

A Maxent model [8, 11] was used to model the current distribution of C. felis in Australia. A total of 179 sam-ples were used, which included samsam-ples obtained in this study, unpublished data and published data (Additional file 2: Table S4). Latitude and longitude coordinates for each sample were entered into Biodiversity and Climate Change Virtual Laboratory (BCCVL) (BCCVL, Griffith University) as biological data [16]. “Australia, Current Climate (1976–2005), 30  arcsec (~1  km)” climate and environmental data was selected from the datasets avail-able in the BCCVL collections. All variavail-ables were initially included in the model, while only the variables with the highest probability of C. felis presence in response to eco-geographical variables were included in the final model as they reported the greatest amount of the observed var-iation. The chosen response variables were required to be within the environmental thresholds for C. felis survival. Namely, temperatures between 3–35  °C with 70–95% humidity and high precipitation levels (> 500 mm yearly) [17, 18]. Receiver operating characteristics (ROC) curves were assessed, where the area under the curve (AUC) was used to evaluate the accuracy of the resulting model. A model with an AUC score of 0.5 or below indicated that the model performed no better than random. Mod-els with an AUC score of 1 indicated a perfect model. Additionally, the variable importance function was used to calculate the correlation score between the standard prediction and the new prediction, giving an estima-tion (%) of the importance of that variable in the model. The higher the value of the variable, the more influential it was in the model. The correlation matrix was used to complement the variable importance function where it showed the probability of predictor variables to be corre-lated to ensure that the included variables are not highly correlated and produce a bias output in the model. It is important to note that there are limitations involved in strictly using AUC models, and they should be used in conjunction with other model evaluation methods [19]. Therefore, we used the variable importance function and correlation matrix with the AUC scores to determine the model of best-fit for the current distribution of C. felis.

Maxent modelling of predicted future distribution of C. felis in Australia under IPCC climate change models

The species distribution models were analysed further using a Maxent climate change model in BCCVL for pre-dicted future distribution of C. felis in Australia. Four IPCC Representative Concentration Pathways (RCP) (2.6, 4.5, 6.0 and 8.5) for the 2050s and 2070s were evaluated: WorldClim, future projection using IPSL-CM5A-LR

RCP2.6 (IMAGE [20]), 10 arcmin (2050), WorldClim, future projection using IPSL-CM5A-LR RCP4.5 (CGAM [21]), 10 arcmin (2050), WorldClim, future projection using IPSL-CM5A-LR RCP6.0 (AIM [22]), 10 arcmin (2050), WorldClim, future projection using IPSL-CM5A-LR RCP8.5 (MESSAGE [23]), 10 arcmin (2050), World-Clim, future projection using IPSL-CM5A-LR RCP2.6, 10 arcmin (2070), WorldClim, future projection using IPSL-CM5A-LR RCP4.5, 10 arcmin (2070), WorldClim, future projection using IPSL-CM5A-LR RCP6.0, 10 arc-min (2070), WorldClim, future projection using IPSL-CM5A-LR RCP8.5, 10 arcmin (2070). The change in area was calculated by examining centre of range, contraction and expansion of the range.

Results

Three divergent cox1 haplogroups of C. felis are present throughout the north‑eastern region of Australia

Cat fleas, C. felis, were genotyped using the mtDNA 5’-end of the cox1 gene (601 bp). Genotyping of C. felis

(n= 81) collected from nine locations in north-eastern region of Australia revealed six cox1 haplotypes (h1–6; Fig. 1, Additional file 1: Table  S3). The majority of the fleas were either haplotype h1 (n= 14, 17.28%) or h4 (n= 55, 67.90%). Pairwise comparison between haplo-types h1 and h4 revealed 97.18% identity (15 nt differ-ences). The six haplotypes clustered into three different clades: Clade ‘Sydney’, Clade ‘Darwin’ and Clade ‘Cairns’. Clade ‘Sydney’ forms a haplogroup of haplotypes h1 (n= 14) and h2 (n= 4) that differ by a single synony-mous nucleotide polymorphism (SNP). Clade ‘Darwin’ is formed from a single haplotype, h3 (n= 5), and is diver-gent from Clade ‘Sydney’ with nucleotide variations at 6 and 5 of 601 positions when compared to haplotypes h1 and h2, respectively. Clade ‘Cairns’ forms a haplogroup of haplotypes h4 (n= 55), h5 (n= 1) and h6 (n= 2) that differ by a SNP and is divergent from Clade ‘Sydney’ and Clade ‘Darwin’. The cox1 amino acid sequences of all clades are 100% identical.

Species distribution modelling confirms a geographical niche for Clade ‘Cairns’ and the nation‑wide distribution of Clade ‘Sydney’

(Fig. 2). The AUC for Clade ‘Sydney’, Clade ‘Darwin’, Clade ‘Cairns’ and all haplotypes were 0.96, 0.99, 1.0 and 0.98, respectively. The variable importance function iden-tified that the maximum temperature of warmest month, mean temperature of coldest quarter, precipitation of wettest quarter and precipitation of warmest quarter variables had an importance of 10%, 40%, 25% and 25%, respectively, in the model. The correlation matrix showed that precipitation of wettest quarter and precipitation of warmest quarter are highly correlated (0.5) whereas all other variables are uncorrelated with each other.

Areas that had a suitability >  50% for Clade ‘Sydney’, Clade ‘Darwin’ and Clade ‘Cairns’ had a maximum tem-perature of 35  °C, 40  °C and 35  °C, respectively, in the warmest month, mean temperature of 10 °C, 15 °C and 25 °C, respectively, in the coldest quarter, precipitation of 250 mm, 1700 mm and 500 mm, respectively, during the wettest quarter and lastly, a precipitation of 1400  mm, 1400 mm and 1500 mm, respectively, during the warmest quarter (Fig. 2). These conditions fall within the required thresholds for survival of C. felis. Clade ‘Sydney’ was observed to be found along the entirety of east coast of Australia, extending to the coast of South Australia, Tas-mania and Perth (Fig. 2). Areas with suitability for the Clade ‘Darwin’ were primarily found along the northern

coastline of Australia, the north to middle parts of the east coast and the western coast of Tasmania (Fig. 2). In contrast, suitable habitats for Clade ‘Cairns’ were primar-ily found in the northern and north-eastern tropical areas of Australia, in particular Townsville, Cairns and the sur-rounding region (Fig. 2).

Modelling of potential future distribution predicts the range of C. felis in Australia to shift south along the eastern coastal regions

Areas with suitable climatic conditions for C. felis in Aus-tralia have been predicted to decrease by 2050 and even further by 2070 under all four RCP scenarios (2.6, 4.5, 6.0 and 8.5; Table 1). Currently, 959,040.82  km2 _is

suit-able for C. felis in Australia. However, in 2050 the suit-able area reduced in all four scenarios, ranging between 548,751.36–680,130.58 km2_{, leaving 54.45–68.61% of the}

area in common with the current model (Table 1, Fig. 3). By the 2070s, the area of suitability declined even fur-ther in all four models with 386,233.19–717,111.65 km2

suitable for C. felis, leaving 27.82–70.26% of the area in common with the current model (Table 1, Fig. 3). The contracted areas are found in the current northern parts of the C. felis range where the geometric centre of the species range shifted 397.14  km south along the

‘Sydney’

‘Darwin’

‘Cairns’

C. canis 80

0.01

Ctenocephalides felis h4

h2 h1 h3

h6 h5

‘Cairns’ ‘Darwin’ ‘Sydney’

10 km

a b

c

east coast by the 2050s (Table 1; Fig. 3). This southward shift is observed to be a further 127.47 km by the 2070s (Table 1, Fig. 3).

Similar results were seen amongst the three indi-vidual clades where the area of suitable climatic con-ditions for survival of C. felis haplotypes declined by 2050 and further by 2070. In 2050 and 2070 respec-tively, 590,190.26–752,174.58  km2 _{and 307,663.81–}

788,241.66 km2 _{out of the current 1,069,926.97 km}2 _area

is suitable for Clade ‘Sydney’ haplogroup (Table 1). The predicted distribution has a similarity of 59.27–71.61%

and 27.83–70.26% in 2050 and 2070, respectively, to the current model (Table 1, Fig. 4). This resulted in a subsequent shift rate of 122.11 km south per dec-ade, with loss of the current northern range (Table 1, Fig. 4). Clade ‘Darwin’ is predicted to experience loss in suitable area, where 123,710.58–185,542.80 km2 _and

141,895.55–210,040.59  km2 _{in 2050 and 2070}

respec-tively, out of the current 169,781.22  km2 _{is suitable}

(Table 1). The predicted distribution has a similarity of 62.55–82.93% and 68.70–82.30% in 2050 and 2070, respectively, to the current suitable area for C. felis

a b

c d

probability

0 .25 .5 0.75 1

Ctenocephalides felis _{Ctenocephalides felis ‘Sydney’}

Ctenocephalides felis ‘Darwin’ Ctenocephalides felis ‘Cairns’

(Table 1, Fig. 5). This resulted in a subsequent shift rate of 49.25  km south per decade (Table 1, Fig. 5). Clade ‘Cairns’ has similarly observed a loss in suit-able area, with a loss of 67,394.81–105,437.14 km2 _and

49,855.41–120,210.54 km2 _{of the current 99,703.03 km}2

range in 2050 and 2070, respectively (Table 1). The pre-dicted distribution has a similarity of 49.97–70.96% and 43.28–74.55% in 2050 and 2070, respectively, to the current suitable area for C. felis (Table 1, Fig. 6). This resulted in a southward range shift of 97.71 km per dec-ade for Cldec-ade ‘Cairns’, with loss of the current northern range (Table 1, Fig. 6).

Discussion

This study has doubled the number of fleas genotyped in Australia and provided an updated perspective on the diversity of C. felis, particularly in the north-east-ern region. Only three cox1 haplotypes have previously been reported from 47 C. felis specimens collected from domestic cats and dogs across Australia [1, 2, 5, 7]. This study confirms the presence of the haplotypes (h1, h4 and h5) previously genotyped, and uncovers the existence of three new cox1 haplotypes (h2, h3 and h6) in north-east-ern Australia. These results provide strong evidence sup-porting intra-specific diversification of C. felis between

Table 1 Summary of climate change scenarios on Ctenocephalides felis in Australia

Note: Total area predicted to be occupied at > 50% probability, distance from each projected centroid and rate per decade of habitat change Scenario Current area lost

(km2₎ Area of _{expansion from}

current area (km2₎

% change in

area Area common to current (km2₎ % current _distribution

retained

Distance to current centroid (km)

Rate of habitat change (km/ decade)

2050: All RCP2.6 301,018.50 22,108.26 29.08 658,022.32 68.61 242.25 75.70 RCP4.5 381,786.81 17,326.07 38.00 577,255.01 60.19 271.92 84.98 RCP6.0 331,719.37 33,929.15 31.05 627,322.45 65.41 338.55 105.80 RCP8.5 436,877.55 26,587.09 42.78 522,164.27 54.45 397.14 124.11 2050: Clade

‘Sydney’ RCP2.6 339,388.78_{RCP4.5 439,006.97} 21,636.39_11,379.71 29.70_39.97 730,538.19_630,919.96 68.28_65.79 215.18_264.77 67.24_82.74 RCP6.0 383,161.11 26,691.03 33.32 686,765.86 71.61 295.67 92.40 RCP8.5 501,527.03 21,790.32 44.84 568,399.94 59.27 391.65 122.39 2050: Clade

‘Darwin’ RCP2.6 55,972.30_{RCP4.5 29,695.90} 24,097.10_45,457.57 18.77_9.28 113,808.92_140,085.23 67.03_82.93 93.97_157.61 29.37_49.25 RCP6.0 63,586.33 17,515.69 27.14 106,194.89 62.55 56.51 17.70 RCP8.5 40,364.56 51,701.02 6.68 129,416.66 76.23 128.77 40.24 2050: Clade

‘Cairns’ RCP2.6 47,923.57_{RCP4.5 28,949.99} 16,947.30_34,684.10 31.07_5.75 51,779.46_70,753.04 51.93_70.96 206.82_252.40 64.50_78.88 RCP6.0 49,881.97 17,574.75 32.40 49,820.06 49.97 132.11 41.28 RCP8.5 49,642.17 29,042.64 20.66 50,060.86 50,21 312.68 97.71 2070: All RCP2.6 280,744.69 38,814.52 25.23 678,297.13 70.72 232.17 44.65 RCP4.5 426,441.54 18,276.39 42.56 532,600.28 55.53 343.84 66.12 RCP6.0 478,536.97 15,717.72 48.26 480,504.85 50.10 353.93 68.06 RCP8.5 589,158.53 16,349.90 59.73 369,883.29 38.57 524.61 100.89 2070: Clade

‘Sydney’ RCP2.6 318,234.54_{RCP4.5 495,955.62} 36,549.23_12,628.19 26.33_45.17 751,692.43_573,971.35 70.26_53.65 218.69_332.05 42.06_63.86 RCP6.0 526,910.57 10,408.90 48.27 507,016.40 47.39 347.37 71.99 RCP8.5 672,242.71 9979.55 61.90 297,684.26 27.82 521.00 100.19 2070: Clade

‘Darwin’ RCP2.6 30,060.54_{RCP4.5 52,684.02} 70,319.91_24,798.35 23.71_16.42 139,720.68_117,097.20 82.30_68.70 132.10_131.59 25.40_25.31 RCP6.0 50,754.84 41,335.67 55.48 119,026.38 70.11 151.47 29.13 RCP8.5 51,142.07 17,440.52 19.85 118,639.16 69.88 169.62 32.62 2070: Clade

a

Ctenocephalides felis

2050

Ctenocephalides felis

2070

RCP6.0

RCP6.0

RCP2.6

RCP4.5

RCP8.5

RCP2.6

RCP4.5

RCP8.5

a

Ctenocephalides felis ‘Sydney’

2050

Ctenocephalides felis ‘Sydney’

2070

RCP6.0

RCP6.0

RCP2.6

RCP4.5

RCP8.5

RCP2.6

RCP4.5

RCP8.5

a

Ctenocephalides felis

‘Darwin’

2050

Ctenocephalides felis

‘Darwin’

2070

RCP6.0

RCP6.0

RCP2.6

RCP4.5

RCP8.5

RCP2.6

RCP4.5

RCP8.5

a

Ctenocephalides felis

‘Cairns’

2050

Ctenocephalides felis ‘Cairns’

2070

RCP6.0

RCP6.0

RCP2.6

RCP4.5

RCP8.5

RCP2.6

RCP4.5

RCP8.5

the north-eastern region and middle to southern regions of Australia. As haplotypes h4, h5 and h6 have only been detected in this tropical region and differ genetically by one SNP, they have been categorised as Clade ‘Cairns’, whilst genetically similar haplotypes h1 and h2 have been found elsewhere have been grouped as Clade ‘Sydney’.

The findings from this study suggest a range expansion of tropical haplogroups as only Clade ‘Sydney’ haplo-group was previously observed in the surrounding area of Cairns in 2014 [1, 2]. However, the theory of emerging haplotypes is questionable as the one dog that was sam-pled in the outer area of Cairns may not have presented the emerging haplotypes [1, 2]. It was unexpected to observe haplotype h3 in the Cairns region as previously it has only been found in Galiwinku, near Darwin (our unpublished data). Clade ‘Darwin’ may have been pre-sent throughout the northern tropical regions before this study and not sampled as only 25 samples have been pre-viously genotyped in these regions.

An initial bottleneck restricting gene flow of the flea populations into Australia could have been the cause of the low haplotype diversity currently present [24]. Over time, the result of extensive transportation and the move-ment of cats and dogs has facilitated interaction between flea populations [25]. Additionally, the abundance of feral cats and dogs could expedite greater genetic trans-fer between flea populations [25]. Despite an increase in diversity suggested by this study, it still reveals relatively low mitochondrial variability and highly restricted haplo-group populations of C. felis in Australia. The finding of six mtDNA haplotypes is considered to be unusually low compared to other flea species, such as the ten haplotypes of Pulex simulans and 24 haplotypes of Oropsylla hirsuta, the prairie dog flea [26, 27]. It is expected that for at least every ten samples of mtDNA sequences greater than 500 bp (e.g. cox1), multiple haplotypes are expected for one species of animal [28]. Nevertheless, low mitochondrial variability has also been observed in other arthropod spe-cies [29]. High homology was similarly found at the cox1 and cox2 mtDNA regions in a study of Anopheles ste-phensi steste-phensi, an important malarial vector in India [29]. Oshaghi et al. [29] suggested the low genetic varia-tion is a result of unrestricted gene flow due to the lack of geographical barriers. This, along with extensive move-ment of hosts, could be the potential contributing factor for the low genetic variation found within Australia [30].

The extensive movement of host allows indirect disper-sal of fleas over a large range; however, the results from this study and two previous studies [1, 2] suggest three genetically distinct haplogroups of C. felis in Australia. These genetically distinct groups indicate a lack of gene flow between some populations [31]. The species diversi-fication is likely to be influenced by climatic variation as

climatic differences can impede gene flow despite suffi-cient opportunity for dispersal from frequent movement of hosts [4].

The model for the present distribution of C. felis in Aus-tralia shows that the most suitable habitat is located along the coastline as it presents the ideal environment for flea survival. The environmental conditions of the eastern coast of Australia consists of moderate to warm tempera-tures and high levels of precipitation that are within the critical thresholds for C. felis survival (Australian Bureau of Meteorology, Australian Government; http://www. bom.gov.au/iwk/clima te_zones /map_1.shtml ) [17, 18]. The Clade ‘Darwin’ model revealed that the range of hap-lotype h3 is along the northern coastal environments. This model for Clade ‘Darwin’ requires additional sam-ples from these remote and scarcely populated areas to be included to further refine the model. Ctenocephalides felis

does not have the ability survive and develop in tempera-tures greater than 35 °C as is seen in inland regions [32].

The predictive models indicate that there is a tropical ecological niche for Clade ‘Cairns’ and Clade ‘Darwin’, whereas Clade ‘Sydney’ has the ability to inhabit most Australian climates. Species diversification as a result of climate as a natural barrier has been observed in other species. The climatic variation between the northern and southern part of Fukushima and Ibaraki prefectures in Japan, with mean temperatures of 18.3  °C and 17  °C respectively, is thought to be the reason for the presence of two genetically distinct groups of the sorghum plant bug, Stenotus rubrovittatus [33]. Australia has a very variable climate across the continent where the northern region presents a tropical climate that transitions into a temperate climate in the southern states (Australian Bureau of Meteorology, Australian Government; http:// www.bom.gov.au/). Fleas dispersed from host movement may not survive, reproduce or parasitise hosts outside their origin due to movement to a new unfavourable hab-itat [34].

however, the positive association between temperature and developmental rate may be offset by the species total bioclimatic requirement for survival [36]. Initially, the increased temperatures may promote the spread and occurrence of C. felis along the north-eastern coastline, but the expected temperature increase of 1.1–6.4 °C from 1980 to 2099 will exceed critical threshold temperatures (35 °C) for C. felis survival in the current northern areas of habitat [37]. As a result, the climatic requirements for the growth and development of C. felis will become lim-ited in these areas and consequently restrict the distribu-tion of the parasite to areas further south with sufficient bioclimatic resources [37]. Climate change in the future is also expected to increase precipitation and humidity lev-els in some areas while other areas will experience severe drought conditions [38]. It is known that flea infestations are mostly absent in the Australian inland communities as drought conditions are too harsh for flea survival [39]. As C. felis development and survival is highly depend-ent on moist environmdepend-ents, distribution is most likely to be found in those regions [17]. As moist regions are becoming further restricted to coastlines in the future, the model suggests that there will be an increase in flea populations in these areas.

Conclusions

A change in the status quo of C. felis genetic structure will be seen where tropical haplogroups may out-perform or displace the temperate haplogroups further south. Under the proposed IPCC climate change scenarios, a south-ward shift of C. felis range within Australia will occur. Predictive models for the spread of species have been proven to be beneficial epidemiological tools in disease control programs [9, 40, 41]. To gain a better understand-ing into intraspecific biological variations and ecology of the haplotypes of C. felis, it will be necessary to directly compare the development of genetically defined C. felis

strains under laboratory conditions with defined biocli-matic variables [42, 43].

Additional files

Additional file 1: Table S1. Summary of Ctenocephalides felis specimens collected in Cairns and the surrounding region. Table S2. Supplementary dataset of Ctenocephalides felis samples collated and used in this study.

Table S3. Summary of Ctenocephalides felis, characterised morphologically and genotyped using the mtDNA cox1 region.

Additional file 2: Table S4. Longitude/latitude of the included Cteno-cephalides felis samples.

Additional file 3: Figure S1. Bioclimatic response graphs for Ctenocephal-ides felis in Australia.

Abbreviations

cox1: cytochrome c oxidase subunit 1 gene; mtDNA: mitochondrial DNA; Max-ent: Maximum Entropy; IPCC: Intergovernmental Panel on Climate Change; RCP: Representative Concentration Pathways; cox2: cytochrome c oxidase subunit 2 gene; PCR: polymerase chain reaction.

Acknowledgements

We thank Graeme Brown (Sydney School of Veterinary Science, University of Sydney), Lee-Anne Kingston (Southside Veterinary Surgery), Jess Wargent (Southside Veterinary Surgery), Paul Matthews (Redlynch Valley Vets), Siobhan Kehoe (Pyramid Veterinary Surgery) as well as veterinarians and veterinary nurses that donated the specimens.

Funding

This study was supported by the Sydney School of Veterinary Science, Univer-sity of Sydney, through the internal support for the honours project of NC.

Availability of data and materials

Nucleotide sequence data from this study are available in the GenBank (National Center for Biotechnology Information, NCBI) database under acces-sion numbers MK093987-MK094067. The datasets analysed during the present study are available in the LabArchives repository, http://dx.doi.org/10.25833 / ncjt-eh29.

Authors’ contributions

NC and JŠ participated in the study design. NC performed DNA isolation, performed the conventional PCR, analysed the data and wrote the draft. NC and JŠ edited the manuscript. Both authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable. Parasites were provided by the veterinary practitioners once removed as part of routine veterinary practice and approval was not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in pub-lished maps and institutional affiliations.

Received: 26 November 2018 Accepted: 13 March 2019

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